Sugar Modification of Wall Teichoic Acids Determines Serotype-Dependent Strong Biofilm Production in Listeria monocytogenes
ABSTRACT Biofilm production is responsible for persistent food contamination by Listeria monocytogenes, threatening food safety and public health. Human infection and food contamination with L. monocytogenes are caused primarily by serotypes 1/2a, 1/2b, and 4b. However, the association of biofilm pr...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2022-10-01
|
| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02769-22 |
| _version_ | 1828100426677878784 |
|---|---|
| author | Myungseo Park Jinshil Kim Liz Horn Jisun Haan Ali Strickland Victoria Lappi David Boxrud Craig Hedberg Sangryeol Ryu Byeonghwa Jeon |
| author_facet | Myungseo Park Jinshil Kim Liz Horn Jisun Haan Ali Strickland Victoria Lappi David Boxrud Craig Hedberg Sangryeol Ryu Byeonghwa Jeon |
| author_sort | Myungseo Park |
| collection | DOAJ |
| description | ABSTRACT Biofilm production is responsible for persistent food contamination by Listeria monocytogenes, threatening food safety and public health. Human infection and food contamination with L. monocytogenes are caused primarily by serotypes 1/2a, 1/2b, and 4b. However, the association of biofilm production with phylogenic lineage and serotype has not yet been fully understood. In this study, we measured the levels of biofilm production in 98 clinical strains of L. monocytogenes at 37°C, 25°C, and 4°C. The phylogenetic clusters grouped by core genome multilocus sequence typing (cgMLST) exhibited association between biofilm production and phylogenetic lineage and serotype. Whereas clusters 1 and 3 consisting of serotype 4b strains exhibited weak biofilm production, clusters 2 (serotype 1/2b) and 4 (serotype 1/2a) were composed of strong biofilm formers. Particularly, cluster 2 (serotype 1/2b) strains exhibited the highest levels of biofilm production at 37°C, and the levels of biofilm production of cluster 4 (serotype 1/2a) strains were significantly elevated at all tested temperatures. Pan-genome analysis identified 22 genes unique to strong biofilm producers, most of which are related to the synthesis and modification of teichoic acids. Notably, a knockout mutation of the rml genes related to the modification of wall teichoic acids with l-rhamnose, which is specific to serogroup 1/2, significantly reduced the level of biofilm production by preventing biofilm maturation. Here, the results of our study show that biofilm production in L. monocytogenes is related to phylogeny and serotype and that the modification of wall teichoic acids with l-rhamnose is responsible for serotype-specific strong biofilm formation in L. monocytogenes. IMPORTANCE Biofilm formation on the surface of foods or food-processing facilities by L. monocytogenes is a serious food safety concern. Here, our data demonstrate that the level of biofilm production differs among serotypes 1/2a, 1/2b, and 4b depending on the temperature. Furthermore, sugar decoration of bacterial cell walls with l-rhamnose is responsible for strong biofilm production in serotypes 1/2a and 1/2b, commonly isolated from foods and listeriosis cases. The findings in this study improve our understanding of the association of biofilm production with phylogenetic lineage and serotype in L. monocytogenes. |
| first_indexed | 2024-04-11T08:28:28Z |
| format | Article |
| id | doaj.art-f35f17376fbe45a597ab83f84121813e |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-11T08:28:28Z |
| publishDate | 2022-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-f35f17376fbe45a597ab83f84121813e2022-12-22T04:34:37ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-10-0110510.1128/spectrum.02769-22Sugar Modification of Wall Teichoic Acids Determines Serotype-Dependent Strong Biofilm Production in Listeria monocytogenesMyungseo Park0Jinshil Kim1Liz Horn2Jisun Haan3Ali Strickland4Victoria Lappi5David Boxrud6Craig Hedberg7Sangryeol Ryu8Byeonghwa Jeon9Division of Environmental Health Sciences, School of Public Health, University of Minnesota, Minneapolis, Minnesota, USADepartment of Food and Animal Biotechnology, Research Institute of Agriculture and Life Sciences, and Center for Food and Bioconvergence, Seoul National University, Seoul, Republic of KoreaPublic Health Laboratory, Minnesota Department of Health, Saint Paul, Minnesota, USAPublic Health Laboratory, Minnesota Department of Health, Saint Paul, Minnesota, USADivision of Environmental Health Sciences, School of Public Health, University of Minnesota, Minneapolis, Minnesota, USAPublic Health Laboratory, Minnesota Department of Health, Saint Paul, Minnesota, USAPublic Health Laboratory, Minnesota Department of Health, Saint Paul, Minnesota, USADivision of Environmental Health Sciences, School of Public Health, University of Minnesota, Minneapolis, Minnesota, USADepartment of Food and Animal Biotechnology, Research Institute of Agriculture and Life Sciences, and Center for Food and Bioconvergence, Seoul National University, Seoul, Republic of KoreaDivision of Environmental Health Sciences, School of Public Health, University of Minnesota, Minneapolis, Minnesota, USAABSTRACT Biofilm production is responsible for persistent food contamination by Listeria monocytogenes, threatening food safety and public health. Human infection and food contamination with L. monocytogenes are caused primarily by serotypes 1/2a, 1/2b, and 4b. However, the association of biofilm production with phylogenic lineage and serotype has not yet been fully understood. In this study, we measured the levels of biofilm production in 98 clinical strains of L. monocytogenes at 37°C, 25°C, and 4°C. The phylogenetic clusters grouped by core genome multilocus sequence typing (cgMLST) exhibited association between biofilm production and phylogenetic lineage and serotype. Whereas clusters 1 and 3 consisting of serotype 4b strains exhibited weak biofilm production, clusters 2 (serotype 1/2b) and 4 (serotype 1/2a) were composed of strong biofilm formers. Particularly, cluster 2 (serotype 1/2b) strains exhibited the highest levels of biofilm production at 37°C, and the levels of biofilm production of cluster 4 (serotype 1/2a) strains were significantly elevated at all tested temperatures. Pan-genome analysis identified 22 genes unique to strong biofilm producers, most of which are related to the synthesis and modification of teichoic acids. Notably, a knockout mutation of the rml genes related to the modification of wall teichoic acids with l-rhamnose, which is specific to serogroup 1/2, significantly reduced the level of biofilm production by preventing biofilm maturation. Here, the results of our study show that biofilm production in L. monocytogenes is related to phylogeny and serotype and that the modification of wall teichoic acids with l-rhamnose is responsible for serotype-specific strong biofilm formation in L. monocytogenes. IMPORTANCE Biofilm formation on the surface of foods or food-processing facilities by L. monocytogenes is a serious food safety concern. Here, our data demonstrate that the level of biofilm production differs among serotypes 1/2a, 1/2b, and 4b depending on the temperature. Furthermore, sugar decoration of bacterial cell walls with l-rhamnose is responsible for strong biofilm production in serotypes 1/2a and 1/2b, commonly isolated from foods and listeriosis cases. The findings in this study improve our understanding of the association of biofilm production with phylogenetic lineage and serotype in L. monocytogenes.https://journals.asm.org/doi/10.1128/spectrum.02769-22Listeriabiofilmsserotypecell wallrhamnosylation |
| spellingShingle | Myungseo Park Jinshil Kim Liz Horn Jisun Haan Ali Strickland Victoria Lappi David Boxrud Craig Hedberg Sangryeol Ryu Byeonghwa Jeon Sugar Modification of Wall Teichoic Acids Determines Serotype-Dependent Strong Biofilm Production in Listeria monocytogenes Microbiology Spectrum Listeria biofilms serotype cell wall rhamnosylation |
| title | Sugar Modification of Wall Teichoic Acids Determines Serotype-Dependent Strong Biofilm Production in Listeria monocytogenes |
| title_full | Sugar Modification of Wall Teichoic Acids Determines Serotype-Dependent Strong Biofilm Production in Listeria monocytogenes |
| title_fullStr | Sugar Modification of Wall Teichoic Acids Determines Serotype-Dependent Strong Biofilm Production in Listeria monocytogenes |
| title_full_unstemmed | Sugar Modification of Wall Teichoic Acids Determines Serotype-Dependent Strong Biofilm Production in Listeria monocytogenes |
| title_short | Sugar Modification of Wall Teichoic Acids Determines Serotype-Dependent Strong Biofilm Production in Listeria monocytogenes |
| title_sort | sugar modification of wall teichoic acids determines serotype dependent strong biofilm production in listeria monocytogenes |
| topic | Listeria biofilms serotype cell wall rhamnosylation |
| url | https://journals.asm.org/doi/10.1128/spectrum.02769-22 |
| work_keys_str_mv | AT myungseopark sugarmodificationofwallteichoicacidsdeterminesserotypedependentstrongbiofilmproductioninlisteriamonocytogenes AT jinshilkim sugarmodificationofwallteichoicacidsdeterminesserotypedependentstrongbiofilmproductioninlisteriamonocytogenes AT lizhorn sugarmodificationofwallteichoicacidsdeterminesserotypedependentstrongbiofilmproductioninlisteriamonocytogenes AT jisunhaan sugarmodificationofwallteichoicacidsdeterminesserotypedependentstrongbiofilmproductioninlisteriamonocytogenes AT alistrickland sugarmodificationofwallteichoicacidsdeterminesserotypedependentstrongbiofilmproductioninlisteriamonocytogenes AT victorialappi sugarmodificationofwallteichoicacidsdeterminesserotypedependentstrongbiofilmproductioninlisteriamonocytogenes AT davidboxrud sugarmodificationofwallteichoicacidsdeterminesserotypedependentstrongbiofilmproductioninlisteriamonocytogenes AT craighedberg sugarmodificationofwallteichoicacidsdeterminesserotypedependentstrongbiofilmproductioninlisteriamonocytogenes AT sangryeolryu sugarmodificationofwallteichoicacidsdeterminesserotypedependentstrongbiofilmproductioninlisteriamonocytogenes AT byeonghwajeon sugarmodificationofwallteichoicacidsdeterminesserotypedependentstrongbiofilmproductioninlisteriamonocytogenes |